The ecological diversification and evolution of Teleosauroidea (Crocodylomorpha, Thalattosuchia), with insights into their mandibular biomechanics

Abstract Throughout the Jurassic, a plethora of marine reptiles dominated ocean waters, including ichthyosaurs, plesiosaurs and thalattosuchian crocodylomorphs. These Jurassic ecosystems were characterized by high niche partitioning and spatial variation in dietary ecology. However, while the ecological diversity of many marine reptile lineages is well known, the overall ecological diversification of Teleosauroidea (one of the two major groups within thalattosuchian crocodylomorphs) has never been explored. Teleosauroids were previously deemed to have a morphologically conservative body plan; however, they were in actuality morphofunctionally more diverse than previously thought. Here we investigate the ecology and feeding specializations of teleosauroids, using morphological and functional cranio‐dental characteristics. We assembled the most comprehensive dataset to date of teleosauroid taxa (approximately 20 species) and ran a series of principal component analyses (PC) to categorize them into various feeding ecomorphotypes based on 17 dental characteristics (38 specimens) and 16 functionally significant mandibular characters (18 specimens). The results were examined in conjunction with a comprehensive thalattosuchian phylogeny (153 taxa and 502 characters) to evaluate macroevolutionary patterns and significant ecological shifts. Machimosaurids display a well‐developed ecological shift from: (1) slender, pointed tooth apices and an elongate gracile mandible; to (2) more robust, pointed teeth with a slightly deeper mandible; and finally, (3) rounded teeth and a deep‐set, shortened mandible with enlarged musculature. Overall, there is limited mandibular functional variability in teleosaurids and machimosaurids, despite differing cranial morphologies and habitat preferences in certain taxa. This suggests a narrow feeding ecological divide between teleosaurids and machimosaurids. Resource partitioning was primarily related to snout and skull length as well as habitat; only twice did teleosauroids manage to make a major evolutionary leap to feed distinctly differently, with only the derived machimosaurines successfully radiating into new feeding ecologies.


| INTRODUC TI ON
Throughout the Mesozoic Era, a plethora of anatomically diverse marine reptiles dominated the oceans (Pyenson et al., 2014). During the Jurassic, three distantly related groups coexisted, sharing the top tiers of the marine trophic webs, ichthyosaurs, plesiosaurs (plesiosauroids and pliosaurids) and thalattosuchians (a group of extinct marine crocodylomorphs) (Benson & Druckenmiller, 2012;Foffa et al., 2018;Massare, 1987Massare, , 1988. Pioneering work by Massare (1987) assigned these extinct marine reptiles to broad ecological guilds (pierce, general, cut, smash, crunch, and crush) based on tooth morphology, but these were qualitative in nature and not universally accepted (Buchy, 2010). More recently, Foffa et al. (2018) examined the dentition of fossil marine reptiles over an approximately 18-million-year history of the Jurassic Sub-Boreal Seaway (United Kingdom) to evaluate feeding ecology using a quantitative approach, validating the guild structure used by Massare (1987). Foffa et al. (2018)'s results showed that extinct marine reptile groups did not significantly overlap in guild space, indicating that dietary niche partitioning allowed many species to coexist.
While the dataset of Foffa et al. (2018) included a wide variety of marine reptile species, there were only a few representatives from Teleosauroidea. Teleosauroids are one of the two main groups within Thalattosuchia, a major radiation of marine crocodylomorphs that were abundant during the Jurassic and Early Cretaceous (the other being the metriorhynchoids, which by the Middle Jurassic gave rise to Metriorhynchidae, the first archosaurs to adopt a fully pelagic lifestyle) Wilberg et al., 2019;Young et al., 2010). Teleosauroids were a near-globally distributed and ecologically diverse clade that inhabited freshwater, brackish, lagoonal and deep-water marine ecosystems (Buffetaut, 1982;Foffa et al., 2019;Johnson et al., 2017Johnson et al., , 2019Johnson et al., , 2020Martin et al., 2016;Young et al., 2014). They used to be regarded as merely marine analogues of extant gavials, based on most species having dorsally directed orbits, an elongate and tubular snout and high tooth count, suggesting that they fed primarily on small, swift-moving prey (Andrews, 1909(Andrews, , 1913Buffetaut, 1982;Hua, 1999).
Here, we rectify this gap and examine the dentition (the most common marine reptile fossils) and mandibular characteristics to evaluate the feeding ecology of teleosauroids, using quantitative methodology as in Foffa et al. (2018) and Foffa (2018). Notably, we expand the teleosauroid dataset substantially from that used in Foffa et al. (2018) and Foffa (2018) for a more comprehensive, indepth evaluation of their feeding ecology.
enable comparisons and detect possible lags in evolution between the mandible and dentition (see Foffa, 2018). In addition, multiple teleosauroid tooth specimens were more readily available than complete mandible specimens, which furthered our intention to keep the datasets separate to avoid possible skewed results. The teleosauroid specimens in the datasets are sampled across their entire evolutionary history, from the Early Jurassic (Plagiophthalmosuchus gracilirostris: lower Toarcian) to the Early Cretaceous (Machimosaurus rex: late Hauterivian/early Barremian) (Data S2). Thus, the specimens come from a wide array of localities and lithological facies, with representatives from four different habitats: freshwater, implied semiterrestrial, coastal marine and lagoonal/pelagic (see Data S2 for more details). This extensive range of taxa and environments allows for an overall greater evaluation and understanding of teleosauroid ecology as a group.
For the dentition dataset, we scored four continuous and 13 discrete characters for each specimen (Data S3; Table 1), modified from Foffa et al. (2018). Teleosauroids display homodont dentition across the entirety of the mandible; therefore, all tooth crowns in our dataset are the largest tooth found in the anterior section of the tooth row, as in Foffa et al. (2018), for consistency. For the mandible dataset, we scored 16 continuous characters (Data S3; Table 2) for near-complete or completely preserved mandibles, using the methods found in Foffa (2018). Measurements were taken directly from specimens using digital calipers, excluding curvature and crown angles (C3 and C4; Data S1) and verified on photographs using ImageJ (Schneider et al., 2012). Dental curvature and crown angles were measured using the angle tool in ImageJ (Abramoff et al., 2004;Schneider et al., 2012).
The jaws of crocodylomorphs (and indeed all tetrapods with a simple jaw joint) act as a simple lever for both opening and closing processes (Ballell et al., 2019;Bestwick et al., 2021;Cleuren & Vree, 2000;Sinclair & Alexander, 1987). The efficacy of such lever can be evaluated using mechanical advantage. In simple levers, such as jaw-systems, mechanical advantage (MA) is the ratio of in-lever length (moment arm of the muscle) divided by out-lever length (distance from the jaw condyle to the biting point) and indicates the proportion of muscle adductor force is transmitted at the bite point (Greaves, 1983;Morales-García et al., 2021;Radinsky, 1981;Stubbs et al., 2013;Westneat, 2003). It is important to note that this metric does not take into account size and that teleosauroids have a large range of values due to the significant variation in snout length and supratemporal muscle size (the influence of size in feeding behavior are further discussed below).

| Multivariate analyses
Before analyses, all continuous characters of both tooth and mandible datasets, were standardized using z-transformation (distributions were equalized to the same mean value, μ = 0, and standard devia- for size variation. Both taxon-character matrices (Data S1) were then transformed into a Gower distance matrix, which allows for the combination of ordered discrete and continuous characters (Gower, 1971). The dental dataset was subjected to both a Principal Component Analysis (PC) and Principal Coordinates Analysis (PCo) in PAST v4.06 (Hammer et al., 2001) following Foffa et al. (2018) and the mandibular dataset was subjected to a PC analysis, to ordinate taxa and produce a plotted morphospace, based on the first two axes (PC1 and PC2 and PCo1 and PCo2, respectively) which represented the highest variation. We included a PCo analysis for the dental dataset as this type of analysis is useful when dealing with discrete characters (Zuur et al., 2007). The mandibular dataset was run a second time with the removal of mandibular length (ML) to assess whether this character influenced the results.

| Evolutionary analyses in relation to phylogeny
A simple time-calibrated phylogenetic tree, centered on a comprehensive, updated phylogenetic analysis of Teleosauroidea (Johnson et al., 2020) was generated in RStudio v3.4.2 using the R packages phytools 0.6 (R Core Team, 2020; Revell, 2012) and ape 4.1 (Paradis et al., 2004) (Data S4). Function DatePhylo (method = "equal") of the package strap (Bell & Lloyd, 2015) was are compatible together and characterize functional mandibular properties; and (3) represent simple lever mechanics (Anderson et al., 2011;Anderson & Friedman, 2012;Stubbs et al., 2013). In these analyses, the anterior-posterior length of muscle attachments (maL/ML; which can be measured in extinct taxa) is used as proxy for adductor muscle force (Busbey, 1989;Porro et al., 2011;Sellers et al., 2017). For each feature, the phylogeny was pruned of the tips for which said feature is unavailable.

| Dentition and mandible
PC1 is largely related to the presence of pseudodenticles, anastomosed pattern and apex shape (37.02%) while PC2 is largely associated with apicobasal crown length (23.82%) (Figure 2). PC1 and PC2 ( Figure 2) show that machimosaurin specimens (Yvridiosuchus, Lemmysuchus, Machimosaurus) are clustered together and largely distinct from all other teleosauroid taxa; this is due to their TA B L E 1 List of continuous (C) and discrete (D) morphological characters used to characterize teleosauroid dentition (modified from Foffa et al., 2018).

Character type Description
Continuous (

C2
Relative length of the symphyseal mandibular area (MSL/ML)

C3
Relative depth of the symphyseal area (MSD/ML)

C4
Depth at the posterior end of the tooth row (eTRD/ ML)

C7
Relative length of the tooth row (TRL/ML)

C8
Relative length of the retroarticular process (RPL/ML)

C16
Tooth index 2 (TI2 = CH/ASDm) distinctive tooth characteristics, such as their conical shape, blunt apices, and pronounced enamel ornamentation (composed of numerous tightly packed ridges in the basal and mid-crown regions, but an anastomosed pattern at the apex) (Young et al., , 2015. In contrast, there is greater overlap between teleosaurids and nonmachimosaurin machimosaurids ( Figure 2). In general, the dentitions PCo1 is largely related to dental ornamentation, apex shape, and tooth curvature (38.05%) and PCo2 is described as apicobasal crown height (12.88%) ( Figure 3). As with the PC analysis, machimosaurins (which is placed phylogenetically closest to machimosaurins; see Johnson et al., 2020), is nearest to machimosaurins along both PC1 and PC2 ( Figure 4). When mandibular length was removed, the overall distribution of the taxa in the morphospace did not change. As with the dentition, the results of the mandibular analysis do not correspond to the six osteological ecomorphotypes (Johnson et al., 2020) discussed above.
Anterior mechanical advantage (

| Biomechanical implications
With regards to our tooth analyses Machimosaurini mostly separate from all other teleosauroids along both PC1 and PC2 and PCo1 and PCo2, consistent with the results in Foffa et al. (2018). This result is expected, given the distinctive tooth morphology of machimosaurins compared with other teleosauroids (e.g., pronounced enamel ornamentation including an apical anastomosed pattern, conical shape, and blunt apex) (Johnson et al., 2017;Young et al., 2014Young et al., , 2015.
Non-machimosaurin machimosaurids were spread out across PCA2, whereas most teleosaurids were restricted to the negative PC1 and PC2 regions of morphospace; however, there was significant overlap between these two groups, regardless of habitat, location or geological age. Our results suggest that groups other than machimosaurins may have had overlapping feeding strategies, despite different habitats and osteological skull and mandibular features. The teleosaurid Mystriosaurus and the machimosaurid Neosteneosaurus are situated most closely to Machimosaurini along PC1 (Figure 2), which may be due to these taxa having large, robust teeth while maintaining a relatively pointed apex.
In our mandibular results, there is a clear evolutionary trend along PC1 from slender mandibles with relatively small adductor muscles (low maL/ML) and short muscle attachment sites ("gracile jaw type"; Figures 9 and 10a) to shorter, broader mandibles with relatively large muscle attachment sites (high maL/ML) ("robust jaw type"; Figures 9 and 10b). Mechanically, small muscle attachment site values generally allow for a higher biting efficiency due to the last tooth being closer to the mandibular musculature; the long distance of the outlever arm of the opening mechanical advantage (oMA) ultimately produces a faster bite. The "gracile jaw type" therefore provides a larger surface area for puncturing prey when biting, increasing the speed of attack and prey capture success rate (Ballell et al., 2019;Pierce et al., 2008;Stubbs et al., 2021;Taylor, 1987). A relatively long tooth row often, but not always, corresponds to a shorter adductor muscle attachment size which contributes to an overall weaker bite (Stubbs et al., 2021).
"Gracile" jaws ( Figure Figures 9 and 10a) can also experience, and have reduced resistance to, increased stress, torsion and bend-  Thorbjarnarson, 1990), and their lower jaws are structurally resistant, capable of feeding on large loads (Ballell et al., 2019). Overall size is a key factor that influences how strong an individual's bite is and the types of prey they can consume, as discussed below. Within teleosauroids, the "gracile jaw type" (slender; high efficiency; fast but weak bite) is present in Plagiophthalmosuchus, most teleosaurids and early diverging non-machimosaurine machimosaurids (Macrospondylus and Charitomenosuchus) (Figure 2). These taxa also have the least optimized out-lever in the lower jaw. The anterior jaw is where maximal loads are dealt with (Wroe et al., 2005) and is therefore important when processing prey items. Plagiophthalmosuchus, most teleosaurids, and smaller individuals of Macrospondylus and Charitomenosuchus display a relatively weaker anterior mechanical advantage (aMA), suggesting that, while they were able to quickly grab prey items, it may have taken time to properly subdue and process them.
The curvature of the posterior portion of the mandible also provides insight into biomechanical adaptations. In machimosaurins (Yvridiosuchus, Lemmysuchus and Machimosaurus), the posterior half of the lower jaw is sharply dorsally curved (Johnson et al., 2017). This may be due to three possible adaptations for increasing bite force: (1) enlarging the size of muscle attachment sites; (2) re-orientating the pterygoideus muscles; and (3) increasing gape. In addition, retroarticular process length and orientation are crucial to bite force, as it is the insertion site for two important jaw muscles (musculus depressor mandibulae and musculus pterygoideus ventralis;  and acts as a major anatomical in-lever in crocodylomorphs (Gignac & O'Brien, 2016). Biting performance decreases as gape increases (Herring & Herring, 1974;Jessop et al., 2006), and therefore macropredatory taxa tend to exhibit adaptations for higher biting performances at wider gapes (Herring & Herring, 1974). A wider gape is also needed when consuming larger prey items. This is observed in metriorhynchids such as Dakosaurus, Tyrannoneustes and Plesiosuchus , which exhibit three main characteristics that infer increased performance during wide gape biting; (1) shortening the rostrum, which increases MA of the adductors; (2) enlarging the supratemporal fenestrae, which increases adductor muscle force magnitude; and (3) high tooth crown development, which increases shearing surface area Young et al., 2010Young et al., , 2013. Crucially, one key feature that enabled certain teleosauroids, including machimosaurins, to achieve macropredator status was their large body and head sizes, as discussed below.
When referring to opening mechanical advantage (oMA), a low value is indicative of a jaw optimized for closing speed and a high value indicates a jaw specialized for biting force (Morales-García et al., 2021). Overall, mechanical advantage effectively offers a continuum between velocity and force. It is important to note that extant crocodylians possess hypertrophied pterygoideus, allowing for fast closure of the jaws and very high bite forces. However, the muscular architecture of thalattosuchians was probably quite different compared with modern crocodylians; thalattosuchian lateral pterygoid flanges are much smaller, and the pterygoideus muscles were likely less developed than in Crocodylia. In general, Plagiophthalmosuchus and teleosaurids have a lower opening mechanical advantage and anterior mechanical advantage and higher posterior mechanical advantage, indicating jaws optimized for closing quickly (Figures 7 and 8). In general, derived machimosaurids (particularly the machimosaurins) have a higher opening mechanical advantage and anterior mechanical advantage and lower posterior mechanical advantage, signifying jaws that close slowly but with heavy force behind them.

| Teleosauroid evolutionary ecology
Overall, our analyses show that the mandibles of both Teleosauridae and Machimosauridae (excluding Machimosaurini) performed similarly, suggesting that there was not a major feeding ecology divide F I G U R E 9 Simplified teleosauroid evolutionary tree with time-calibrated geological scale displaying six different ecomorphotypes within Teleosauroidea and different ecotype divergences within Machimosauridae. For ecomorphotypes: green represents longirostrine specialist; light blue represents pelagic form; yellow represents macrophage/durophage form; brown represents semi-terrestrial form; purple represents longirostrine generalist; orange represents mesorostrine generalist; and black represents unknown. For machimosaurid ecotypes: circle represents ecotype 1; triangle represents ecotype 2; star represents ecotype 3 (with [left] corresponding tooth and [right] mandible silhouettes, in which a question mark represents unknown). The box shows hypothesized prey items. Silhouettes provided by PhyloPic© by Spotila, K. Sorgan, I. Braasch, E. Schumacher, C. Cevrim, and H. Filhol.
between the two groups ( Figure 9). This is particularly evident in the long-snouted forms and presents an interesting parallel with the study of Johnson et al. (2020), in where the authors found multiple distinguishing features within the crania and postcrania of most genera, but relatively few distinctive mandibular characteristics (aside from the dentition). This suggests that, at least in terms of feeding, teleosauroids (excluding Machimosaurini and close relatives) remained relatively conservative, with limited mandibular functional diversity.
Overall, the mandibles of most teleosaurids and basal machimosaurids do not show any significant differences, as most taxa retained an elongated, slender mandible with pointed teeth that was ideal for catching small, fast prey (Figure 9; Drumheller & Wilberg, 2020). It is curious that while no great variation is observed in mandibular mechanics amongst the long-snouted forms, many of them (particularly teleosaurid taxa) were living in different habitats, such as semi-marine (e.g., Charitomenosuchus), pelagic (e.g., Aeolodon), freshwater (e.g., Indosinosuchus) and more terrestrial (e.g., Platysuchus) (Foffa et al., 2019;Johnson et al., 2020;Martin et al., 2019). This suggests the possibility that teleosaurids and basal machimosaurids where generally either feeding in a similar manner or on similar prey types but in different habitats, and that habitat preference, in addition to snout length and size, was likely a major driver in resource partitioning, rather than mandibular functionality. Amongst these long-snouted taxa, Mycterosuchus exhibits an optimal jaw type for catching fast-moving prey. A combination of an extremely elongated mandible, small muscle attachments and comparatively low opening mechanical advantage, as well as slender, curved, pointed teeth, suggest that it was specialized in catching quick prey items such as fishes. However, and intriguingly, within teleosaurids Indosinosuchus taxa are more closely positioned to basal machimosaurids on PC1 (see Figure 5). This may be due to these taxa having a slightly shorter and deeper jaw than other teleosaurids. In Jurassic lower Phu Kradung Formation in northeastern Thailand (Johnson et al., 2020;Martin et al., 2019), and a differing oMA could possibly suggest nice partitioning within teleosauroid species found in the same environment.
As mentioned previously, long-snouted basal machimosaurids (e.g., Macrospondylus, Charitomenosuchus) exhibit similar feeding styles to teleosaurids, but derived non-machimosaurine machimosaurids (e.g., Proexochokefalos and Neosteneosaurus) show signs of the mandible switching to a diet not necessarily requiring speed or high bite efficiency but rather capable of subduing larger, specialized prey (e.g., increased musculature, shortening and posterodorsal curvature of the jaw, stress resistant). These taxa also compensated for their relatively slower bite, low bite efficiency and limited biting space by having shortened and robust jaws and increased muscle adductor areas, which were better suited for feeding on potentially slower but more heavily armored prey. Our analyses suggest that there were three machimosaurid ecotypes while Proexochokefalos cf. bouchardi (ecotype 2) is extremely rare (Johnson et al., 2020). In addition, machimosaurin taxa made up for a relatively slower and lower biting efficiency by growing to large sizes, as discussed below.
As discussed previously, Proexochokefalos had a mandible well adapted for tackling large prey, with some of the largest muscle attachment sites (shared with Neosteneosaurus) and opening mechanical advantage within teleosauroids (Figure 7), near equal to Machimosaurus. Importantly, Vignaud (1995), Foffa (2018)  During the Late Jurassic, there was a diverse assemblage of eucryptodiran turtles (Anquetin et al., 2014;Joyce et al., 2021;Püntener et al., 2015), particularly in Europe. Bite marks and embedded teeth suggest that Lemmysuchus and Machimosaurus specialized in macrophagy/durophagy, feeding on larger, armored prey such as turtles and scaled fishes (Meyer, 1988;Young et al., 2014;. It is possible that early machimosaurines began to successfully exploit these prey types, evolving the necessary mandibular tools (short and broad jaws, large muscles, high bite force, and wider gape) to successfully overpower them. Interestingly, our analyses suggest that characteristics toward macrophagy/durophagy in the teleosauroid mandible evolved first (e.g., deep, robust jaws; shortened mandibular symphysis; shortened and curved retroarticular process), with specific tooth characteristics (e.g., blunt apex; little to no curvature; conspicuous enamel ornamentation) evolving afterwards. In certain areas, such as Morocco and Switzerland, machimosaurids are found alongside turtle plastrons with machimosaurid teeth embedded in them (Meyer, 1991;Young et al., 2014).

| Macrophagy in teleosauroids
Large size is beneficial for macropredation, as it allows an animal to feed upon a multitude of different-sized prey items (particularly larger and more energetically feasible ones) and reduces the time taken to process prey (Verwaijen et al., 2002). In general, larger animals, as well as animals with large heads, bite harder (Verwaijen et al., 2002) and are more resistant to stresses (Ballell et al., 2019).
Large head and body size also compensates for a slower bite or lower biting efficiency by increasing the proportions, strength and mass of an animal. Machimosaurins represent some of the largest teleosauroids in terms of body size, with some Machimosaurus taxa reaching over 7 m in length (Young et al., 2016). This implies that, despite a quantitatively slower bite, in absolute terms machimosaurins were still able to seize prey relatively quickly and efficiently due to their massive bulk, in addition to biting harder and processing food quicker.
During teleosauroid evolution, there was an independent shift toward big body size/head size in both teleosaurids and machimo-

| CON CLUS ION
Historically, the ecology of teleosauroids has been considered conservative (Andrews, 1913;Buffetaut, 1982). However, recent papers discussing specific teleosauroid habitats and osteological ecomorphotypes (Foffa et al., , 2019Johnson et al., 2020;Martin et al., 2016) show that teleosauroid ecology is more complex than originally thought. We provide an ecological quantitative assessment of teleosauroids by using tooth and mandibular measurements, following the methods used by Foffa (2018) and Foffa et al. (2018). The results of our tooth analysis are similar, but greatly expand to those found in Foffa et al. (2018), in which members of Machimosaurini and machimosaurids (e.g., Macrospondylus, Neosteneosaurus, machimosaurins). Ultimately, there is not a great deal of mandibular variability in teleosaurids and machimosaurids (despite differing habitat preferences in certain taxa), suggesting a subtle feeding ecological divide between the two groups. Resource partitioning was primarily related to snout and skull length as well as habitat; only twice (from ecotype 1 to 2 and ecotype 2 to 3) did teleosauroids manage to make a major evolutionary leap to feed distinctly differently, with only the derived machimosaurines successful in radiating into new feeding ecologies.

ACK N OWLED G M ENTS
The authors would like to sincerely thank two anonymous review- Evers for discussion on turtle evolution. Open Access funding enabled and organized by Projekt DEAL.

CO N FLI C T O F I NTE R E S T
The authors declare no competing interests.

O PE N R E S E A RCH BA D G E S
This article has earned an Open Data badge for making publicly available the digitally-shareable data necessary to reproduce the reported results. The data is available at http://osf.io.

DATA AVA I L A B LI LIT Y S TATEM ENT
The authors declare that all the data supporting the findings of this study are available within the paper and its supplementary data files.

S U PP O RTI N G I N FO R M ATI O N
Additional supporting information can be found online in the Supporting Information section at the end of this article.